Expression of nitric oxide synthase during germ cell apoptosis in testis of cynomolgus monkey after testosterone and heat treatment

Journal of Andrology

Volumn 30, Issue 2, 2009, Pages 190-199

  Guo, Jian ^a,b   Jia, Yue ^c   Tao, Shi Xin ^a   Li, Yin Chuan ^a   Zhang, Xue Sen ^a   Hu, Zhao Yuan ^a   Chiang, Naomi ^c   Lue, Yan He ^c   Sinha Hikim, Amiya P ^c   Swerdloff, Ronald S ^c   Wang, Christina ^c   Liu, Yi Xun ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b BEIJING UNIVERSITY OF CHINESE MEDICINE   (China)

^c HARBOR UCLA MEDICAL CENTER   (United States)

Author keywords

43 C water bath; Andrology; INOS

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; SILASTIC; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; GERM CELL; HORMONE INHIBITION; HYPERTHERMIC THERAPY; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MALE; MONKEY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; SERTOLI CELL; SPERMATOGONIUM; TEMPERATURE MEASUREMENT; TESTIS BIOPSY; TESTIS CELL; THERMAL EXPOSURE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; GENE EXPRESSION; HOT TEMPERATURE; IMMUNOHISTOCHEMISTRY; MACACA FASCICULARIS; MALE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; SPERMATOZOA; TESTIS; TESTOSTERONE;

EID: 62649129016     PISSN: 01963635     EISSN: None     Source Type: Journal    
DOI: 10.2164/jandrol.108.005538     Document Type: Article

References (47)

1. Adams ML, Meyer ER, Sewing BN, Cicero TJ. Effects of nitric oxide-related agents on rat testicular function. J Pharmacol Exp Ther. 1994;269:230-217.
2. Bardin CW, Cheng CY, Musto NA, Gunsalus GL. The Sertoli cell. In: Knobil E, Neill JD, Ewing LL, Greenwald GS, Markert CL, Pfaff DW, eds. The Physiology of Reproduction. New York: Raven Press: 1988;933-974.
3. Beck KF, Eberhardt W, Frank S, Huwiler A, Mebmer UK, Muhl H, Pfeilschifter J. Inducible NO synthase: role in cellular signaling. J Exp Biol. 1999;202:645-653.
4. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton S. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci U S A. 1995;92:7162-7166.
5. Chen BW, Sun BN, Shang EN, Shen HM. The therapeutic effect to β-NGF on AD models in rats. J Clin Exp Med. 2006:5:1477-1480.
6. Chen ZP, Mitchelhill KI, Michell BJ, Stapleton D, Rodriguez-Crespo I, Witters LA, Power DA, Ortiz de Montellano PR, Kemp BE. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett. 1999;443:285-289.
7. Drew B, Leeuwenburgh C. Aging and the role of reactive nitrogen species. Ann N Y Acad Sci. 2002;959:66-81.
8. Griswold MD. The central role of Sertoli cells in spermatogenesis. Semin Cell Dev Biol. 1998;9:411-416.
9. Griswold MD, Morales C, Sylvester SR. Molecular biology of the Sertoli cell. Oxf Rev Reprod Biol. 1988;10:124-161.
10. Guo CX, Ma J, Zhou XC, Liu YX. Expression of hSP 70-2 gene during germ cell apoptosis in rat unilateral cryptorchid testes. Arch Androl. 2000;46:109-115.
11. Hofmann F, Ammendola A, Schlossmann J. Rising behind NO: cGMP-dependent protein kinases. J Cell Sci. 2000;113:1671-1676.
12. Jia Y, Sinha Hikim AP, Lue YH, Swerdloff RS, Vera Y, Zhang XS, Hu ZY, Li YC, Liu YX, Wang C. Signaling pathways for germ cell death in adult cynomolgus monkeys (Macaca fascicularis) induced by mild testicular hyperthermia and exogenous testosterone treatment. Biol Reprod. 2007;77:83-92.
13. Kostic TS, Andric SA, Maric D, Kovacevic RZ. Inhibitory effects of stress-activated nitric oxide on antioxidant enzymes and testicular steroidogenesis. J Steroid Biochem Mol Biol. 2000;75:299-306.
14. Kostic TS, Andric SA, Maric D, Stojilkovic SS, Kovacevic R. Involvement of inducible nitric oxide synthase in stress-impaired testicular steroidogenesis. J Endocrinol. 1999;163:409-416.
15. Lee VY, McClintock DS, Santore MT, Scott Budinger GR, Chandel NS. Hypoxia sensitizes cells to nitric oxide-induced apoptosis. J Biol Chem. 2002;277:16067-16074.
16. Lue Y, Hikim APS, Wang C, Leung A, Swerdloff RS. Functional role of inducible nitric oxide synthase in the induction of male germ cell apoptosis, regulation of sperm number, and determination of testes size: evidence from null mutant mice. Endocrinology. 2003;144: 3092-3100.
17. Lue Y, Wang C, Liu YX, Sinha Hikim AP, Zhang XS, Ng CM, Hu ZY, Li YC, Leung A, Swerdloff RS. Transient testicular warming enhances the suppressive effeci of testosterone on spermatogenesis in adult cynomolgus monkeys (Macaca fascicularis). J Clin Endocrinol Metab. 2006;91:539-545.
18. Lue YH, Sinha Hikim AP, Swerdloff RS, Im P, Taing KS, Bui T, Leung A, Wang C. Single exposure to heat induces stage-specific germ cell apoptosis in rats: role-of intratesticular testosterone on stage specificity. Endocrinology. 1999;140:1709-1717.
19. McLachlan RI, O'Donnell L, Meachem SJ, Stanton PG, De Kretser DM, Pratis K, Robertson DM. Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Rec Prog Horm Res. 2002;57:149-179.
20. Mu X, Liu Y, Collins LL, Kim E, Chang O. The p53/retinoblastoma-mediated repression of testicular orphan receptor-2 in the rhesus monkey with cryptorchidism. J Biol Chem. 2000;275:23877-23883.
21. Narula A, Gu YQ, O'Donnell L, Stanton PG, Robertson DM, McLachlan RI, Bremner WJ. Variability in sperm suppression during testosterone administration to adult monkeys is related to follicle stimulating hormone suppression and not to intratesticular androgens. J Clin Endocrinol Metab. 2002;87:3399-3406.
22. O'Bryan MK, Schlatt S, Gerdprasert O, Phillips DJ, de Kretser DM, Hedger MP. Inducible nitric oxide synthase in the rat testis: evidence for potential roles in both normal function and inflammation mediated infertility. Biol Reprod. 2000a;63:1285-1293.
23. O'Bryan MK, Schlatt S, Phillips DJ, de Kretser DM, Hedger MP. Bacterial lipopolysaccharide-induced inflammation compromises testicular function at multiple levels in vivo. Endocrinology. 2000b:141:238-246.
24. Pentikaainen V, Dunkel L, Erkkila K. Male germ cell apoptosis. Endocr Dev. 2003;5:56-80.
25. Shao L, Tanaka T, Gribi R, Yu J. Thioredoxin-related regulation of NO/ NOS activities. Ann N Y Acad Sci. 2002:962:140-150.
26. Sharma AC, Sam AD, Lee LY, Hales DB, Law WR, Ferguson JL, Bosmann HB. Effect of NG-nitro-L-arginine methyl ester on testicular blood flow and serum steroid hormones during sepsis. Shock. 1998:9:416-421.
27. Sinha Hikim AP, Luc Y, Diaz Romero M, Yen PH, Wang C, Swerdloff RS. Deciphering the pathways of germ cell apoptosis in the testis. J Steroid Mol Biol. 2003a;85:175-182.
28. Sinha Hikim AP, Lue Y, Yamamoto CM, Vera Y, Rodriguez S, Yen PH, Soeng K, Wang C, Swerdloff RS. Key apoptotic pathways for heat-induced programmed germ cell death in the testes. Endocrinology. 2003b;144:3167-3175.
29. Sinha Hikim AP, Rajavashisth TB, Sinha Hikim I, Lue Y, Bonavera JJ, Leung A, Wang C, Swerdloff RS. Significance of apoptosis in the temporal and stage-specific loss of germ cells in the adult rat after gonadotropin deprivation. Biol Reprod. 1997;57:1193-1201.
30. Sinha Hikim AP, Swerdloff RS. Hormonal and genetic control of germ cell apoptosis in the testis. Rev Reprod. 1999;4:38-47.
31. Tao SX, Guo J, Zhang XS, Li YC, Hu ZY, Han CS, Liu YX. Germ cell apoptosis-induced by experimental cryptorchidism is mediated by multiple molecular pathways in cynomolgus macaclue. Front Biosci. 2006;11:1077-1089.
32. Vera Y, Diaz-Romero M, Rodriguez S, Lue Y, Wang C, Swerdloff RS, Sinha Hikim AP. Mitochondria-dependent pathway is involved in heat-induced male germ cell death: lessons from mutant mice. Biol Reprod. 2004;70:1534-1540.
33. Vera Y, Erkkila K, Wang C, Nunez C, Kyttanen S, Lue Y, Dunkel L, Swerdloff RS, Sinha Hikim AP. Involvement of p38 mitogen-activated protein kinase and inducible nitric oxide synthase in apoptotic signaling of murine and human male germ cells after hormone deprivation. Mol Endocrinol. 2006;20:1597-1609.
34. Vernet D, Bonavera JJ, Swerdloff RS. Gonzales-Cadavid NF, Wang C. Spontaneous expression of inducible nitric oxide synthase (iNOS) in the hypothalamus and other brain regions of aging rats. Endocrinology. 1998;139:3254-3261.
35. Wang C, Cui YG, Wang XH, Jia Y, Sinha Hikim A, Lue YH, Tong JS, Qian LX, Sha JH, Zhou ZM, Hull L, Leung A, Swerdloff RS. Transient scrotal hyperthermia and levonorgestrel enhance testosterone induced spermatogenesis suppression in men through increased germ cell apoptosis. J Clin Endocrinol Metab. 2007;92:3292-3304.
36. Weissman BA, Niu E, Ge R, Sottas CM, Holmes M, Hutson-JC, Hardy MP. Paracrine modulation of androgen synthesis in rat Leydig cells by nitric oxide. J Androl. 2005;26:369-378.
37. Zhang XS, Lue YH, Guo SH, Yuan JX, Hu ZY, Han CS, Hikim AP, Swerdolff RS, Wand C, Liu YX. Expression of HSP105 and HSP60 during germ cell apoptosis in the heat-treated testes of adult cynomolgus inonkeys (Macaca fascicularis). Front Biosci. 2005;10:3110-3121.
38. Zhang XS, Zhang ZH, Guo SH, Yang W, Zhang ZQ, Yuan JX, Jin X, Hu ZY, Liu YX. Activation or extracellular signal-related kinases 1 and 2 in Sertoli cells in experimentally cryptorchid rhesus monkeys. Asian J Androl. 2006a;8:265-272.
39. Zhang XS, Zhang ZH, Jin X, Wei P, Hu XQ, Chen M, Lu CL, Lue YH, Hu ZY, Sinha AP, Swerdloff RS, Wang C, Liu YX. Dedifferentiation of adult monkey Sertoli cells through activation of extracellularly regulated kinase 112 induced by heat treatment. Endocrinology. 2006b;147:1237-1245.
40. Zhang ZH, Jin X, Wei P, Hu ZY, Liu YX Bcl-2 and p53 are involved in experimental cryptorchidism-induced testicular germ cell apoptosis in rhesus monkey. Contraception. 2003a;68:297-301.
41. Zhang ZH, Zhou XC, Wei P, Hu ZY, Liu YX. Expression of BcL-2 and Bax in rhesus monkey testis during germ cell apoptosis induced by testosterone undecanoate. Arch Androl. 2003b;49:439-447.
42. Zhou XC, Han XB, Hu ZY, Zhou RJ, Liu YX. Expression of Hsp70-2 in unilateral cryptorchid testes of rhesus monkey during germ cell apoptosis. Endocrine. 2001a;16:89-95.
43. Zhou XC, Wei P, Hu ZY, Gao F, Zhou RJ, Liu YX Role of Fas/FasL genes in azoospermia or oligozoospermia induced by testosterone undecanoate in rhesus monkey. Acta Pharmacol Sin. 2001b;22: 1028-1033.
44. Zhou XC, Zhang ZH, Hu ZY, Zhou RJ, Liu YX Expression of Hsp 70-2 in rhesus monkey testis during germ cell apoptosis induced by testosterone undecanoate. Contraception. 2002;66:377-382.
45. Zini A, Abitbol J, Girardi SK, Schulsinger D, Goldstein M, Schlegel PN. Germ cell apoptosis and endothelial nitric oxide synthase (eNOS) expression following ischemia-reperfusion injury to testes. Arch Androl. 1998;41:57-65.
46. Zini A, Abitbol J, Schulsinger D, Goldstein M, Schlegel PN. Restoration of spermatogenesis after scrotal replacement of experimentally cryptorchid rat testes: assessment of germ cell apoptosis and eNOS expression. Urology. 1999;53:223-227.
47. Zini A, O'Bryan MK, Magid MS, Schlegel PN. Immunohistochemical localization of endothelial nitric oxide synthase in human testes, epididymis, and vas deferens suggests a possible role for nitric oxide in spermatogenesis, sperm maturation, and programmed cell death. Biol Reprod. 1996;55:935-941.